Tritonia diomedea (Bergh, 1894)[1] is a nudibranch mollusc that has served as a model system for understanding the neural basis of behavior, cellular properties of neurons, and neuromodulation. It is particularly attractive because of the large size of its individual neurons (up to 800 microns), and its large variety of interesting behaviors, eg, escape swimming, magnetic field orientation, rheotaxis, crawling, feeding, mating. Work in the 1960s by A.O. Dennis Willows[2] was among the first to show the functions of single identified neurons in the production of behavior in any organism.

Contents

Species information

Figure 2: Two Tritonia mating.

Of the several "Tritonia" species most of the neurobiological research has been done on Tritonia diomedea. This animal lives in the Pacific Ocean coastal waters from Alaska to California. It feeds on soft coral such as sea pens, sea pansies, and sea whips. Not much is known about the ecology of the animal, but video studies in its natural habitat have contributed to our understanding of natural behavior (Wyeth and Willows, 2006a; Wyeth et al., 2006). As is true of other opisthobranchs, Tritonia is an obligate hermaphrodite, it can act as either male or female and must mate with another individual to reproduce. The sexual organs are located on the right side of the animal, so that animals pull up "starboard to starboard" to mate. They produce egg strands that can be raised in the lab. The eggs hatch to a planktotrophic veliger larva stage.

Figure 3: Schematic of "Tritonia" central ganglia with some neuronal cell bodies marked. Ce=Cerebral Ganglion; Pl=Pleural Ganglion; Pd=Pedal Ganglion Body wall nerves are named after their ganglion of origin plus the number indicated. The identified neurons shown have contralateral counterparts. C1 is a giant serotonergic neuron that projects to the buccal ganglion. C2 is a peptidergic neuron involved in swimming. The cells marked 5,6 are Pedal 5 and 6, which are efferent peptidergic neurons. DSI are the Dorsal Swim Interneurons, a group of three serotonergic neurons in the swim CPG. The statocyst on the right is label, st.

The central nervous system is composed of the circumesophageal ring ganglia: cerebropleural, pedal (Pd), and buccal. The cerebropleural ganglion appears to represent a fusion between the cerebral (Ce) and pleural (Pl) in other opisthobranchs. Although these ganglia are fused, the neurons are often referred to as being in one or the other of the two ganglia.

The central ganglia consist of about 8000 individual neurons (Boyle et al., 1983). Some of these form clusters, others are uniquely identifiable. There are about 180 different types of neuron that have been identified in Tritonia. Notable neurons are shown in Figure 2. A complete list of neurons is cataloged in the "Tritonia" Branch of NeuronBank

Sensory Systems

Tritonia exhibits mechanosensivity and chemosensitivity over the surface of its body. There are sensory neurons with central cell bodies, called S-cells, which are bimodal, mechanoreceptors and chemoreceptors. As with other opisthobranchs, Tritonia has rhinophores that have a chemosensitive function (Wyeth and Willows 2006b).

Tritonia appears to be sensitive to water flow (Field and MacMillan 1973, Willows 1978). It tends to orient its body into the flow of water. The lateral branch of Cerebral Nerve 2 (CeN2) innervates the oral veil and carries information that is necessary (Murray and Willows 1996) for orientation to water flow, so-called rheotaxis.

One of the most striking sensory abilities of Tritonia, is its magnetoreception. Tritonia is capable of sensing Earth-strength magnetic fields and orienting to them. Correspondingly, efferent pedal neurons have been shown to change their firing in response to artificially altering the magnetic field. The mechanism for transduction of this sensory modality has not yet been determined.

Tritonia has no image forming eyes. As with other nudibranchs, it has photosensitive cells that are clustered together in the head region. Not much is known about the eyes (see however, Chase 1974). "Tritonia" also has statocysts that lie adjacent to the connective between the pleural and cerebral ganglia. These have not been examined in "Tritonia". See however, the related nudibranch Hermissenda.

Motor Systems

Motor responses that have been studied in this system include, feeding, gill withdrawal, ciliary locomotion, and swimming. The primary means of locomotion for Tritonia is mucociliary gliding in which the animal secretes mucus upon which it glides due to the action of cilia in the foot. Muscular movements do not seem to play a role in crawling, but may aid in turning (Redondo and Murray 2005). The rate of ciliary beating is controlled by efferent neurons in the pedal ganglia that contain serotonin and/or neuropeptides. In particular, a neuropeptide named Tritonia Pedal Peptide (Tpep) was shown to be released from giant pedal neurons and accelerate ciliary beating. A group of large neurons in the pedal ganglia, in particular, Pd5 and Pd6 are immunoreactive to Tpep.

Figure 4: Tritonia escape swimming. The picture shows a Tritonia escaping from a sea star, Pycnopodia. At the top are simultaneous intracellular electrophysiological recordings from the 3 central pattern generator (CPG) neurons: C2, DSI, and VSI taken from an isolated brain. At the arrow, a body wall nerve was stimulated, producing a pattern of discharges that lasts about a minute. DSI bursts alternate with VSI bursts producing dorsal and ventral body flexions. To the right is the neural circuit from sensory neurons to efferent output.

The other means of locomotion used by Tritonia is escape swimming in which the animal flattens its body (particularly its oral veil and tail) in the horizontal plane, and executes a series of 2-20 alternating dorsal-ventral body flexions. This serves to lift the animal off of the substrate so that water currents can carry it away to safety. The escape swim is performed in response to contact with the predatory sea star, Pycnopodia helianthoides. Tritonia will also swim in response to some other echinoderms, salt crystals or concentrated NaCl, or the bites of conspecifics. The CPG underlying this rhythmic behavior has been well studied. (See: Tritonia swim network). This CPG was one of the first to be reconstructed in realistic computer simulations. The CPG contains just three neuron types: Cerebral Interneuron 2 (C2), Dorsal Swim Interneuron (DSI-A,B,C, and Ventral Swim Interneuron (VSI-B).

The mechanism underlying production of the swim motor pattern is as follows. Sensory activation of the swim motor pattern is mediated by the S-cells. These neurons convey excitation to the Dorsal Ramp Interneuron (DRI) through Tr1, a trigger neuron. DRI, then excites the serotonergic DSIs. The DSIs excite C2 and also modulate its properties, allowing it to further recruit DRI firing. This sets up a positive feedback loop. VSI-B inhibits DSI and C2, momentarily interrupting the cycle. The CPG neurons excite efferent flexion neurons in the pedal ganglion (the dorsal flexion neurons (DFN) and the ventral flexion neurons (VFN)) that relay the activity to the muscles.

Behavioral Plasticity

The Tritonia swim response exhibits a number of forms of behavioral plasticity. When repeatedly stimulated to swim, the animal and the isolated nervous system exhibit habituation, evident by a progressive reduction in flexion cycles per swim. The animal and the isolated nervous system also exhibit sensitization, evident by a period of enhanced swim responsiveness. The Tritonia swim response also exhibits prepulse inhibition, where prior tactile stimulation will briefly suppress the ability of other stimuli to elicit the swim.

Cellular and Synaptic Actions

The DSIs of the swim CPG are serotonergic and have neuromodulatory actions on other members of the swim CPG. This was termed Intrinsic Neuromodulation because the neuromodulation was coming from within the circuit as opposed to from elements outside the circuit. The modulatory actions of the DSIs can be complex, producing what has been called Spike-timing-dependent neuromodulation.